Foreseeing fates: a commentary on Manton (1928) ‘On the embryology of a mysid crustacean,Hemimysis lamornae’

Sidnie Manton became best known for her work on arthropod locomotion, and for proposing radical views on the evolution of arthropods that were accepted for a generation. However, her early training was as an embryologist, and the work that she carried out at the beginning of her career still stands as one of the major twentieth century contributions to the study of crustacean embryology. Here, I review her first major paper, largely completed while she was a graduate student, describing embryonic development in Hemimysis lamornae, a small shrimp-like animal found in the seas around the UK. The clarity of her writing and the quality of her figures set a standard that laid the basis for subsequent work, and although not all of her conclusions have stood the test of time, they remain a standard reference for work today. This commentary was written to celebrate the 350th anniversary of the journal Philosophical Transactions of the Royal Society.     

The clonal composition of biramous and uniramous arthropod limbs

We present the first comparative cell lineage analysis of uniramous and biramous limbs of an arthropod, the crustacean Orchestia cavimana. Via single cell labelling of the cells that are involved in limb development, we are able to present the first complete clonal composition of an arthropod limb. We show that the two main branches of crustacean limbs, exopod and endopod, are formed by a secondary subdivision of the growth zone of the main limb axis. Additional limb outgrowths such as exites result from the establishment of new axes. In contrast to general belief, uniramous limbs in Orchestia are not formed by the loss of the exopod but by suppression of the split into exopod and endopod. Our results offer a developmental approach to discriminate between the different kinds of branches of arthropod appendages. This leads to the conclusion that a 'true' biramous limb comprising an endopod and an exopod might have occurred much later in euarthropod evolution than has previously been thought, probably either in the lineage of the Mandibulata or that of the Tetraconata.     

浙江枝吻纽虫吻的形态学研究

采用组织学、电镜技术等手段对浙江枝吻纽虫吻的生物学特性进行了研究,阐述浙江枝吻纽虫吻的结构与其他分枝纽虫吻的组织结构异同.研究结果表明,浙江枝吻纽虫吻为一条长的肌肉组织的管道结构,一端连着头部组织,一端延伸在一个封闭的空腔中.吻腔环肌层与体壁环肌层没有交叉点,但是吻腔壁背面的环肌与体壁背面的环肌通过一束肌肉而交织在一起.在吻壁处富含大量的分泌细胞和神经细胞.当吻离体后,在普通海水中伸缩能维持 2~4 h.     

Limb morphogenesis in the branchiopod crustacean, Thamnocephalus platyurus, and the evolution of proximal limb lobes within Anostraca

Crustacean limbs exhibit highly diverse morphologies. One major route of diversification is in the number and position of branches arising from the proximal part of the limb. Here I describe development of larvae of the branchiopod crustacean, Thamnocephalus platyurus and describe in detail the development of the thoracic limbs. The thoracic limbs bear proximal branches both medially and laterally. The most proximal branches on either side (gnathobase and pre-epipod) show a similar developmental history: they develop via fusion of two rudiments into a single adult branch. However, phylogenetic analysis suggests that the developmental fusions have distinct evolutionary histories. In one case (gnathobase), the developmental rudiments reflect the ancestral adult morphology of two distinct branches. In the other (pre-epipod), the rudiments are an apparent novelty within the Anostraca and develop into two adult structures in only a single derived family.     

Vergleichende Morphologie des Schmetterlingsrüssels und seiner Sensillen — Ein Beitrag zur phylogenetischen Systematik der Papilionoidea (Insecta, Lepidoptera)

Comparative morphology of the butterfly proboscis and its sensilla — a contribution to the phylogenetic systematics of Papilionoidea (Insecta, Lepidoptera) The morphology of the proboscis was investigated in more than 70 European representatives of Papilionoidea using light microscopy and scanning electron microscopy. The composition of the proboscis wall, its surface structures, as well as the shape and distribution of the different types of sensilla are compared. Special attention is given to the tip region and the diversity of the sensilla styloconica. Plesiomorphic features of the proboscis of Papilionoidea were found to include vertically extended exocuticular ribs composing the galeal wall, cuticular spines restricted to the ventral side of the proximal galea, and two rows of fluted sensilla styloconica restricted to the tip region. Apomorphic features of the proboscis in Papilionidae are three rows of small sensilla styloconica. The presence of cuticular spines all over the galeae was identified as an autapomorphy of Pieridae. Possible apomorphies of Nymphalidae are oblique exocuticular ribs of the galeal wall and the great number and length of the sensilla styloconica (significant at p < 0.01, t-test). A possible synapomorphy of Lycaenidae and Riodinidae are cuticlar spines up to the distal galeae. Distinct transformation series of sensilla styloconica give evidence that divergent evolutionary trends led from fluted shafts to a multitude of other shapes in Papilionidae, Nymphalidae (sensu lato), and Lycaenidae. Long smooth-shafted, club-shaped sensilla styloconica, bearing apical spines, are found in Nymphalinae, Apaturinae and Limenitidinae. Highly derived sensilla styloconica evolved in Heliconiinae and Melitaeini, which are arranged in only one row in both taxa. Their shafts are smooth, flattened and bear an excentral sensory cone. Further apomorphic character states are dented flutes which evolved several times, independently from each other in Satyrinae, Lycaeninae and Riodinidae. The results are discussed in a systematical context and provide the basis for a better understanding of the function of different morphological structures of the proboscis in feeding.     

Integration and dissociation of limb elements in flying vertebrates: a comparison of pterosaurs, birds and bats

Flapping flight has evolved independently in three vertebrate clades: pterosaurs, birds and bats. Each clade has a unique flight mechanism involving different elements of the forelimb. Here, patterns of limb integration are examined using partial correlation analysis within species and matrix correlation analysis across species to test whether the evolution of flapping flight has involved developmental dissociation of the serial homologues in the fore- and hind limb in each clade. Our sample included seven species of birds, six species of bats, and three species of pterosaurs for which sufficient sample sizes were available. Our results showed that, in contrast to results previously reported for quadrupedal mammals, none of the three clades demonstrated significant integration between serial homologues in the fore- and hind limb. Unexpectedly, there were few consistent patterns of within-forelimb correlations across each clade, suggesting that wing integration is not strongly constrained by functional relationships. However, there was significant integration within the hind limbs of pterosaurs and birds, but not bats, possibly reflecting the differing functions of hind limbs (e.g. upright support vs. suspension) in these clades.     

Congruency Effects on Load Bearing in Diarthrodial Joints

Modelling load bearing in diarthrodial joints is challenging, due to the complexity of the materials, the boundary and interface conditions and the geometry. The articulating surfaces are covered with cartilage layers that are filled with a fluid that plays a major role in load bearing [Mow, V.C., Holmes, M.H., Lai, W.M. (1984) “Survey article: fluid transport and mechanical properties of articular cartilage: a review”, Journal of Biomechanics 17(5), 377–394]. Researchers have tended to approximate joint geometry using axisymmetry [Donzelli, P.S., Spilker, R.L., Ateshian, G.A., Mow, V.C. (1999) “Contact analysis of biphasic transversely isotropic cartilage layers and correlations with tissue failure”, Journal of Biomechanics 32, 1037–1047], often with a rounded upper articulating surface, creating a form of Hertz problem [Donzelli, P.S., Spilker, R.L., Ateshian, G.A., Mow, V.C. (1999) “Contact analysis of biphasic transversely isotropic cartilage layers and correlations with tissue failure”, Journal of Biomechanics 32, 1037–1047]. However, diarthrodial joints (shoulder, hip and knee) are equipped with peripheral structures (glenoid labrum, acetabular labrum and meniscus, respectively) that tend to deepen the joint contact and thus cause initial contact to be established at the periphery of the joint rather than “centrally”. The surface geometries are purposefully incongruent, and the incongruency has a significant effect on the stresses, pressures and pressure gradients inside the tissue. The models show the importance of the peripheral structures and the incongruency from a load-bearing perspective. Joint shapes must provide a compromise between demands for load-bearing, lubrication and the supply of nutrients to the chondrocytes of the cartilage and cells of the peripheral structures. Retention and repair of the functionality of these peripheral structures should be a prime consideration in any surgical treatment of an injured joint.     

How reversible is development? Contrast between developmentally plastic gain and loss of segments in barnacle feeding legs

Segmented organisms and structures have fascinated biologists since William Bateson first described homeotic transformation and recognized the fundamental evolutionary significance of segmental organization. On evolutionary time scales, segments may be lost or gained during major morphological transitions. But how segment loss compares to gain on developmental time scales remains mysterious. Here, we examine the ease of reverse development (opposite to normal growth) by comparing developmentally plastic leg segment loss versus gain in individual barnacles transplanted between different water flow conditions. Plastic segment addition occurred rapidly (one to two molts) and exclusively near the limb base. In contrast, developmentally plastic segment loss—the first observation in any arthropod—took much longer (>10 molts) and, remarkably, occurred throughout the leg (23% of losses occurred mid‐limb). Segment loss was not a simple reversal of segment addition. Intersegmental membranes fused first, followed by elimination of duplicate tendons and gradual shortening (but not loss) of duplicate setae. Setal loss, in particular, may impose a severe developmental constraint on arthropod segment fusion. This asymmetric developmental potential (time lag of phenotypic response)—plastic segment addition (amplified normal development) is faster and more orderly than segment loss (reverse development)—adds a new dimension to models of developmental plasticity because the cost of making a developmental mistake in one direction will be greater than in the other.